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The Journal of Neuroscience, February 21, 2007, 27(8):1902-1912; doi:10.1523/JNEUROSCI.5346-06.2007

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Cellular/Molecular
Dominant Role of ß Subunits of G-Proteins in Oxytocin-Evoked Burst Firing

Yu-Feng Wang and Glenn I. Hatton

Department of Cell Biology and Neuroscience, University of California, Riverside, Riverside, California 92521

Correspondence should be addressed to Yu-Feng Wang, Department of Cell Biology and Neuroscience, University of California, Riverside, Riverside, CA 92521. Email: yufengw{at}ucr.edu

Pulsatile neuropeptide secretion is associated with burst firing patterns; however, intracellular signaling cascades leading to bursts remain unclear. We explored mechanisms underlying burst firing in oxytocin (OT) neurons in the supraoptic nucleus in brain slices from lactating rats. Application of 10 pM OT for 30 min or progressively rising OT concentrations from 1 to 100 pM induced burst firing in OT neurons in patch-clamp recordings. Burst generation was blocked by OT antagonist and ionotropic glutamate receptor blockers or tetanus toxin. Blocking G-protein activation with suramin or intracellular GDP-ß-S, but not intracellularly administered antibody against the OT-receptor (OTR) C terminus, blocked bursts. Moreover, pretreatment of slices with pertussis toxin, an inhibitor of G_i/o-proteins, did not block OT-evoked bursts, suggesting that G_i/G_o activation is unnecessary for burst generation. Thus, we further examined G_q/11-associated signaling pathways in OT-evoked bursts. Inhibition of phospholipase C or RhoA/Rho kinase did not block bursts. Activation of Gß subunits using myristoylated Gß-binding peptide (mSIRK) caused bursts, whereas intracellularly loaded antibody against Gß subunit blocked OT-evoked bursts. Blocking Src family kinase, but not phosphatidylinositol 3-kinase, occluded OT-evoked bursts. Similar to the effects of OT on EPSCs, mSIRK inhibited tonic EPSCs and elicited EPSC clustering. Finally, suckling caused dissociation of OTRs and Gß subunits from G_q/11 subunits shown by coimmunoprecipitation and immunocytochemistry, supporting crucial roles for OTRs and Gß subunits in the milk-ejection reflex. We conclude that Gß subunits play a dominant role in burst firing evoked by applied OT or by suckling.

Key words: coimmunoprecipitation; G_q/11 subunit; milk-ejection reflex; oxytocin receptor; signal transduction; Src family kinase

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Received Aug. 17, 2006; revised Jan. 17, 2007; accepted Jan. 18, 2007.

Correspondence should be addressed to Yu-Feng Wang, Department of Cell Biology and Neuroscience, University of California, Riverside, Riverside, CA 92521. Email: yufengw{at}ucr.edu

This article has been cited by other articles:

				Y.-F. Wang and G. I. Hatton Astrocytic Plasticity and Patterned Oxytocin Neuronal Activity: Dynamic Interactions J. Neurosci., February 11, 2009; 29(6): 1743 - 1754. [Abstract] [Full Text] [PDF]

				Y.-F. Wang and G. I. Hatton Interaction of Extracellular Signal-Regulated Protein Kinase 1/2 with Actin Cytoskeleton in Supraoptic Oxytocin Neurons and Astrocytes: Role in Burst Firing J. Neurosci., December 12, 2007; 27(50): 13822 - 13834. [Abstract] [Full Text] [PDF]

				K. J. Iremonger and J. S. Bains Integration of Asynchronously Released Quanta Prolongs the Postsynaptic Spike Window J. Neurosci., June 20, 2007; 27(25): 6684 - 6691. [Abstract] [Full Text] [PDF]

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